Bizzozzero, M. R., Allen, S. J., Gerber, L., Wild, S., King, S. L., Connor, R.C., ... Krützen, M. (2019). Tool use and social homophily among malebottlenose dolphins. Proceedings of the Royal Society B: Biological Sciences,286(1904), [20190898]. https://doi.org/10.1098/rspb.2019.0898

Peer reviewed version

License (if available):Other

Link to published version (if available):10.1098/rspb.2019.0898

Link to publication record in Explore Bristol ResearchPDF-document

This is the accepted author manuscript (AAM). The final published version (version of record) is available onlinevia The Royal Society at https://doi.org/10.1098/rspb.2019.0898 . Please refer to any applicable terms of use ofthe publisher.

University of Bristol - Explore Bristol ResearchGeneral rights

This document is made available in accordance with publisher policies. Please cite only the publishedversion using the reference above. Full terms of use are available:http://www.bristol.ac.uk/pure/about/ebr-terms

Tool use and social homophily among male bottlenose dolphins 1

2

Bizzozzero MR1*, Allen SJ1,2,3, Gerber L1, Wild S4,1, King SL2,3, Connor RC5, Friedman WR6,7, Wittwer S1, Krützen 3

M1. 4

5

1Evolutionary Genetics Groups, Department of Anthropology, University of Zurich, CH-8057 Zurich, Switzerland 6

2School of Biological Sciences, University of Western Australia, Perth, WA 6009, Australia 7

3School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, United Kingdom 8

4School of Biology, University of Leeds, Leeds, LS2 9JT, United Kingdom 9

5Biology Department, University of Massachusetts Dartmouth, North Dartmouth, MA 02747, USA 10

6 Department of Cognitive Science, University of California San Diego, La Jolla, CA 92093, USA 11

7 National Center for Ecological Analysis and Synthesis, University of California Santa Barbara, Santa Barbara, CA 12

*Author for correspondence: manuela.bizzozzero@uzh.com 13

14

15

ABSTRACT に 16

Homophilous behaviour plays a central role in the formation of human friendships. Individuals form 17

social ties with others that show similar phenotypic traits, independently of relatedness. Evidence of 18

such homophily can be found in bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western 19

Australia, where females that use marine sponges as foraging tools often associate with other females 20

that use spongesく け“ヮﾗﾐｪｷﾐｪげ ｷゲ ; ゲﾗIｷ;ﾉﾉ┞ ﾉW;ヴﾐWS, time consuming behaviour, transmitted from mother 21

to calf. Previous research illustrated a strong female bias in adopting this technique. The lower 22

propensity for males to engage in sponging may be due to its incompatibility with adult male-specific 23

behaviours, particularly the formation of multi-level alliances. However, the link between sponging 24

and male behaviour has never been formally tested. Here, we show that male spongers associated 25

significantly more often with other male spongers irrespective of their level of relatedness. Male 26

spongers spent significantly more time foraging, and less time resting and travelling than did male 27

non-spongers. Interestingly, we found no difference in time spent socialising. Our study provides novel 28

insights into the relationship between tool use and activity budgets of male dolphins, and indicates 29

social homophily in the 2nd-order alliance composition of tool using bottlenose dolphins. 30

31

Keywords: bottlenose dolphins, tool use, alliance formation, activity budget, social networks, 32

homophily 33

34

35

INTRODUCTION 36

Individuals acquire information and behavioural skills from conspecifics through social learning across a variety 37

of taxa, including insects, fishes, reptiles, birds and mammals (1に4). Despite the widespread prevalence of 38

social learning, this strategy may not always be beneficial, as knowledge gained from conspecifics can be 39

maladaptive with ﾗﾐWげゲ own behavioural patterns (5). It is therefore important for individuals to learn 40

selectively from others to maximise benefits (6). Explanations for why, when and from whom individuals learn 41

include adopting behaviour performed by the majority (7), behaviour performed by kin (8) or based on 42

increased pay-offs (9), among others (reviewed in (4,10)). However, while social learning has received 43

considerable attention in the literature, relatively little is known about what differences exist between the 44

sexes and what consequences such differences might hold for adult life. 45

Sexual selection theory predicts that males should primarily engage in behaviours related to increasing 46

mating opportunities, while females should invest more in behaviours related to increasing access to resources 47

and offspring protection (11,12). Differences in behavioural requirements or preferences are therefore 48

expected to dictate sex biases in social learning. For example, both male and female chimpanzees (Pan 49

troglodytes) learn socially to insert flexible tools made from vegetation into termite mounds in order to extract 50

termites, yet females learn けデWヴﾏｷデW fishingげ earlier, use it more frequently and do so more efficiently than 51

males (13,14). The differing priorities in learning to use a tool are reflective of the different strategies of male 52

and female chimpanzees to maximise fitness. Chimpanzees use tools in foraging contexts, thus, the benefits of 53

engaging in such a technique should be higher for females than males. Male chimpanzees form coalitions to 54

compete for and maintain alpha male status, a social position that confers increased reproductive opportunity 55

(15). Consequently, males might be less inclined to invest in learning or improving complicated feeding 56

techniques, but rather invest in social relationships with other males (16). 57

In the Indo-Pacific bottlenose dolphin (Tursiops aduncus) population of Shark Bay, Western Australia, 58

sex bias is evident in a socially learned foraging technique involving the use of marine sponges as tools (17,18). 59

Sponge-I;ヴヴ┞ｷﾐｪ ふけゲヮﾗﾐｪｷﾐｪげぶ ｷゲ デｴﾗ┌ｪｴデ デﾗ ヮヴﾗデWIデ デｴW Sﾗﾉヮｴｷﾐげs rostrum while foraging for prey on the sea floor 60

(17,19). Sponging allows these dolphins ふけゲヮﾗﾐｪWヴゲげぶ to exploit a novel ecological niche by providing access to 61

prey not available to those dolphins unfamiliar with tool use (20). Sponging is observed in both the eastern and 62

western gulfs of Shark Bay, but only some members of particular matrilines use sponges (west: approx. 38% of 63

all females (21); east: approx. 13% of all females (22)). This is why sponging is thought to be an exclusively 64

vertically transmitted behaviour (18,23). Around 91% of female calves adopt sponging from their sponging 65

mothers, while only 50% of males do so. The observed female bias in sponging is most likely reflective of a sex 66

bias in social learning propensities at a young age (24に26). 67

Sponging females are distinctive with regards to their activity budget, spending more time foraging 68

and less time resting than their non-sponging female counterparts (21,24). When foraging, female spongers 69

devote 95% of their time to sponging, compared to other foraging behaviours (24). They are also seen alone 70

more often than non-spongers (22,24). However, when associating with other individuals, female spongers 71

show a preference for other sponging females (22). While there is a considerable amount of data on female 72

spongers, much less is known about male spongers. For instance, why proportionally fewer males learn and 73

specialise in this foraging technique, and if and how sponging influences adult male behaviour, remain 74

unknown. The latter is of particular relevance as male dolphins in Shark Bay exhibit one of the most complex 75

social structures outside humans (reviewed in (27)). 76

Bottlenose dolphins in Shark Bay live in an open fission-fusion society with changing group sizes and 77

compositions (27,28). Males form different levels of reproductive alliances with other males, driven by intense 78

competition for access to receptive females (27). Two to three males cooperate in '1st-order' alliances to 79

consort single oestrus females (29). These males also generally associate within larger '2nd-order' alliances 80

comprised of 4-14 individuals, whose members cooperate to take females from rival alliances and to defend 81

against such attacks (29). 1st- and 2nd-order allies are also frequently observed together in non-mating contexts 82

(29). Second-order alliances are considered the stable, core unit of male social organisation in Shark Bay, while 83

the stability of 1st-order alliances varies considerably (27). These complex social relationships among males can 84

ﾉ;ゲデ aﾗヴ SWI;SWゲ ;ﾐS ;ヴW IヴｷデｷI;ﾉ デﾗ W;Iｴ ﾏ;ﾉWげゲ ヴWヮヴﾗS┌Iデｷ┗W ゲ┌IIWゲゲ (27). Alliances are considered costly, as 85

each male must invest time in the formation and maintenance of these relationships (30). 86

Sponging is also a costly behaviour: it requires significant time investment and is associated with a 87

decrease in overall sociability (22,24), as well as less time to rest and travel (21). The investment of time and 88

energy into male alliance behaviours may therefore preclude engaging in time-consuming, solitary foraging 89

techniques, such as sponging. It has been proposed that sponging might put males at a disadvantage in forming 90

and maintaining alliances compared to males that use foraging techniques that are both less time-consuming 91

and less solitary (17,18,21,24). However, these arguments assume that the time, social and energetic demands 92

of sponging on males and females are similar, which has yet to be tested. Here we assess the effect of sponging 93

on male dolphin behaviour by comparing activity budgets, sociability, and association patterns of male 94

spongers to male non-spongers. 95

96

METHODS 97

Study site and data collection 98

Data for this study were collected in the western gulf of Shark Bay, Western Australia, in an area that includes 99

various habitat types, such as seagrass-rich shallow waters (< 10 m) and deep water channels with sandy 100

substrates (> 10 m) (31). We collected behavioural and genetic data during the austral winters from 2007 to 101

2015, identifying individual dolphins by photographs of their dorsal fins (32). During boat-based surveys of 102

dolphin groups, within the first five minutes, we recorded GPS position, environmental parameters (including 103

sea state, water depth and temperature), group size and composition, as well as predominant group activity 104

(rest, travel, forage, socialise, or unknown; cf. (33) and SI). We defined group membership according to the 10 105

m chain rule (33). Male dolphins that had been observed carrying a sponge while foraging at least twice on 106

different days were classified as spongers (24), while males that had never been observed sponging were 107

classified as non-spongers. Individuals that had been observed sponging only once were classified as 108

けunknownsげ. We obtained biopsy samples from dolphins on an opportunistic basis using a purpose-designed 109

system for sampling small cetaceans (34). The samples were used to genetically sex individuals (35) and 110

determine pairwise genetic relatedness (18). Further details of sampling and laboratory methods are provided 111

in the SI. Unless otherwise specified, all analyses were conducted in R V1.1.453 (36). 112

113

Data Restriction 114

We included only independent/weaned males and excluded dependent calves (37). Only males observed more 115

than nine times and identified as spongers or non-spongers were included in our analyses. Sex was identified 116

either genetically (see SI) or behaviourally by several observations of alliance-typical behaviour (being observed 117

regularly travelling side-by-side engaging in synchronous surfacing, consorting of females, or inter-group 118

aggression with other males; cf., (27,38)). Furthermore, in order to assess males with similar association 119

opportunities, we restricted our analyses to comparisons of male spongers with non-sponging males that also 120

met habitat use criteria based on depth and home range overlap derived from data on sponging males. Further 121

details on the calculation of these criteria are provided in the SI. Restricting the data in this manner resulted in 122

a data set containing 37 male dolphins, including 13 spongers and 24 non-spongers. 123

124

Effect of sponging on male activity budgets 125

To investigate differences in activity budgets (proportions of resting, travelling, foraging, and socialising 126

behaviour) between male spongers and non-spongers, we conducted a multivariate analysis of variance 127

(MANOVA) with the sole predictor of whether an individual was classified as sponger or non-sponger 128

(hereafter: foraging technique). As dependent variables, we calculated activity budgets by dividing the number 129

of individual sightings per activity by the total number of individual sightings. We used Pｷﾉﾉ;ｷげゲ デヴ;IW ふVぶ ;ゲ a test 130

statistic due to the unequal sample sizes in our data set (39). To investigate which activity proportions, in 131

particular, differed between male spongers and non-spongers, we performed sequential Bonferroni corrected, 132

post-hoc, independent t-デWゲデゲ ふWWﾉIｴげゲ デ-test, (40)). While investigating the data structure of the multivariate 133

activity budgets, we identified five outliers from the combined normal distribution. Thus, we conducted the 134

MANOVA with outliers removed, retaining 32 males (spongers: n = 12, non-spongers: n = 20) in the data set 135

(see SI for analysis with the full data set). 136

137

Degree of sociability of male spongers and non-spongers 138

To investigate whether male spongers were more or less solitary than male non-spongers, we compared their 139

levels of sociability. We constructed an index of sociability by dividing the number of solitary sightings by the 140

total number of sightings per individual. We compared individual sociability indices of male spongers and male 141

non-spongers in a two-sample permutation test (10,000 permutations) implemented in the けpermげ package 142

(41). 143

To investigate the association pattern of male spongers and male non-spongers, we adhered to the 144

following procedure. First, to maximise our ability to draw comparisons with other studies on cetaceans, we 145

calculated Half Weight Indices (HWIs) as a measure of the proportion of time two males spent together (42). 146

Based on the dyadic HWIs, we created a social network to analyse the association patterns between male 147

spongers and male non-spongers. Second, we assessed whether associations in the social network followed a 148

random pattern or whether two individuals were seen more or less often together than expected by chance 149

(43,44). For this analysis, we specified a daily sampling period. Third, to test whether the association indices 150

between pairs consisting of males with similar foraging techniques (sponger に sponger; non-sponger に non-151

sponger) were higher than between pairs with different foraging techniques (sponger に non-sponger), we 152

carried out a Mantel test on a similarity matrix and the matrix of dyadic associations with 10,000 permutations. 153

The similarity matrix is a 1/0 matrix providing information on whether two individuals belong to the same 154

group (either both spongers or both non-spongers = 1) or to different groups (sponger and non-sponger = 0). 155

These analyses were conducted in SOCPROG 2.6 (45). 156

In a further step, we ran a Double Decker Semi-Partialling Multiple Regression Quadratic Assignment 157

Procedure (MRQAP-DSP; see below and (46)) to investigate whether the documented pattern of dyadic 158

associations (between male pairs of spongers, pairs of non-spongers, and pairs of one sponger and one non-159

sponger) could be predicted by similarity in foraging technique, even when controlling for pairwise relatedness 160

(based on 27 microsatellite loci; see SI for more detailed information). Similarity in foraging technique was 161

presented in two matrices: in the first, we coded similarity in sponging as 1; and vice versa in the second where 162

similarity in non-sponging was coded as 1. Unequal dyads were assigned a value of 0 in both matrices. Separate 163

similarity matrices allowed us to disentangle the contribution of similarity in sponging and non-sponging, 164

respectively, to the association pattern. 165

An MRQAP-DSP test is similar to a partial linear multiple regression with the exception that dependent 166

and predictor variables are presented as matrices. Thus, this method tests whether an entered predictor 167

variable significantly contributes to the explanation of the dependent matrix, whilst controlling for the other 168

predictors. To control for the dependencies between data points, we used the MRQAP-DSP test as 169

implemented and described in the けasnipeげ package (47) using 10,000 permutations. We did not include 170

mitochondrial haplotypes in the predictors due to a previously documented high correlation with foraging 171

technique (48). Only males for which we had genetic data available were included in this test (spongers: n = 9, 172

non-spongers: n = 16). We also repeated the MRQAP-DSP test including all genotyped males within our study 173

population while additionaly correcting for home range overlaps (see SI). 174

To investigate whether the association patterns found in the previous analysis were also reflected in 175

2nd-order alliance compositions, we defined 2nd-order alliances based on dyadic HWIs. We lacked sufficient 176

consortship data to define alliances functionally (i.e., through observation of consortship behaviour) for this 177

study, so we could use only association strength as a proxy (33). We used an average linkage agglomerative 178

cluster analysis assuming a hierarchical social network structure (49) performed in SOCPROG (45) and defined 179

and applied a threshold value at which a dyad can be considered to be part of the same 2nd-order alliance. To 180

find an appropriate threshold, we conducted a change point analysis employing the Pruned Exact Linear Time 181

ふPELTぶ ﾏWデｴﾗS ゲヮWIｷaｷWS ｷﾐ デｴW けIｴ;ﾐｪWヮﾗｷﾐデげ ヮ;Iﾆ;ｪW (50) (cf. (51) and SI for more detailed information). 182

183

RESULTS 184

Between 2007 and 2015, we observed 124 male dolphins at least nine times. After applying the restrictions 185

outlined above imposed, the resulting data set contained 37 male dolphins, of which 13 were spongers and 24 186

were non-spongers (number of sightings: mean = 35; range = 17-68). We computed HWIs from a total of 549 187

survey records over the nine-year study period. All males associated with at least five other individuals in the 188

data set. 189

190

Effect of sponging on male activity budgets 191

We detected significantly different activity budgets between male spongers and non-spongers (V = 0.74, 192

F(4,27) = 19.6, p < 0.001). Thus, foraging techniques significantly contributed to explaining an individual ﾏ;ﾉWげゲ 193

activity budget. Post-hoc analyses showed that male spongers foraged more, and rested and travelled less than 194

male non-spongers. There was no significant difference in time spent socialising between male spongers and 195

non-spongers (Tab. 1). 196

197

Degree of sociability of male spongers and male non-spongers 198

Male spongers were encountered significantly more often alone (sociability index: mean = 0.22, SE = 0.03) than 199

male non-spongers (sociability index: mean = 0.04, SE = 0.01; p = 0.002). 200

Among the 37 males, the overall mean HWI was 0.09 (1,000 bootstraps: SE = 0.03), including the zeros 201

of no associations. Considering only non-zero associations, the more conservative measure, the mean HWI was 202

0.17 (1,000 bootstraps: SE = 0.05). The generated network based on the dyadic association indices (Fig. 1) 203

represented a non-random social structure (10,000 permutations, 1,000 switches; SDobs = 0.17, SDrandom = 0.14, 204

p < 0.001). Thus, some males were observed more often in association than expected by chance alone, 205

reflecting their well-documented alliance associations (27). 206

Association rates between pairs of males with similar foraging techniques (sponger に sponger; non-207

sponger に non-sponger; mean HWI = 0.14, SD = 0.09) were significantly higher (Mantel test, t = 5.75; p < 0.01; 208

Tab. 2) than associations between pairs with different foraging techniques (sponger に non-sponger: mean HWI 209

= 0.05, SD = 0.04). 210

The MRQAP regression model showed that sponging was a significant predictor of male association 211

patterns, even after controlling for relatedness (Tab. 3). Related individuals did not associate above chance 212

levels. These findings were also supported by the results of the MRQAP-DSP tests including all males within our 213

study area (see SI for more information). Our analyses demonstrate that the association pattern of male 214

dolphins inhabiting deep water and occupying similar home ranges can at least partly be explained by foraging 215

technique. 216

An average linkage agglomerative cluster analysis to define 2nd-order alliances resulted in a tree 217

diagram representing the underlying data well with a cophenetic correlation coefficient of 0.98 (45,52). The 218

PELT method resulted ｷﾐ ; Iｴ;ﾐｪW ヮﾗｷﾐデ ;デ HWI д ヰくヲΑく This cut-off value is higher but well within the range of 219

previous findings on the male dolphins of Shark Bay, in which a HWI of 0.20 has commonly been used in 220

assigning males to 2nd-order alliances (27,33). Applying 0.27 as a threshold to define 2nd-order alliances 221

illustrated that the tendency of male spongers to associate with other male spongers was reflected in 2nd-order 222

alliance compositions. We identified nine 2nd-order alliances, of which two consisted exclusively of spongers, 223

one was of mixed composition (sponger and non-sponger) and the other six were composed exclusively of non-224

spongers (Fig. 2). Four individuals (three spongers, one non-sponger) could not be assigned to a 2nd-order 225

alliance. Five of the non-sponging alliances and both sponging alliances have also been observed engaging in 226

functional alliance behaviour, e.g. consorting females. A similar pattern was found when we included all males 227

in our study population (see SI for more detail). 228

229

DISCUSSION 230

It has been hypothesised that the investment of time and energy into the formation and maintenance of male 231

alliances likely reduces the propensity for male dolphins to engage in time-consuming, solitary foraging 232

techniques such as sponging, thereby resulting in the strong female bias previously documented (17,18,21,24). 233

This hypothesis was based on the assumptions that male spongers engage in different activity and social 234

patterns than male non-spongers. Our results support these assumptions by revealing that, at least in the 235

austral winters when data were collected, male spongers differed in their activity budgets, foraging more, and 236

resting and travelling less than male non-spongers. Interestingly, the time spent socialising was equal among 237

male spongers and non-spongers despite the fact that male spongers spent more time alone than male non-238

spongers. When male spongers were observed with other males, they associated significantly more often with 239

other male spongers. 240

Previous studies on female activity budgets in Shark Bay also found that spongers spent a greater 241

proportion of their time foraging and less time resting and travelling than their non-sponging counterparts 242

(21,24), suggesting thattime investment could be a proximate cost of sponging in comparison to other foraging 243

techniques for both sexes. A comparison between the sexes warrants further investigation. Interestingly, 244

socialising proportions for males seem not to be affected by these time investments, suggesting that a 245

comparatively smaller amount of time spent restingmight be the proximate cost of sponging. However, these 246

potential costs might be offset by having fewer competitors for food, as sponging may decrease competition 247

for resources by providing access to a novel ecological niche (19,20). Indeed, the role of intraspecific 248

competition on niche expansion has been reported across several taxa (53,54). 249

Our finding that male spongers and male non-spongers spent equal amounts of time socialising 250

contradicts the hypothesis that sponging conflicts with cooperative male alliance behaviour. However, when 251

comparing sociability, we found that male spongers had higher proportions of solitary sightings compared to 252

male non-spongers. Our findings thereby corroborate previous studies indicating that sponging is a largely 253

solitary activity (21,24). The increased solitariness of male spongers might still affect cooperative male alliance 254

behaviour negatively to some degree, even though there is no difference in socialising time. 255

Our examination of male social structure in deep water habitat revealed that male spongers tended to 256

associate with other male spongers rather than male non-spongers, as demonstrated by their clustering in the 257

social network. Sponging was a significant predictor of the observed association patterns of males sharing 258

similar home ranges even after controlling for pairwise relatedness and similarity in non-sponging. Likewise, 259

when we repeated our analysis and included all genotyped males, similarity in sponging remained a significant 260

predictor for social structuring (see SI for more information). These results contradict a previous study on male 261

dolphins in eastern Shark Bay (22), which did not detect a significant effect of similarity in foraging technique 262

on social structuring. This was most likely a result of low sample size as there are far fewer spongers, and 263

particularly male spongers, in the eastern gulf of Shark Bay compared to the western gulf (22,31). Remarkably, 264

in our study, while similarity in foraging technique was significant in terms of impact on social structuring, 265

pairwise relatedness was not (Tab. 3). The absence of an effect of relatedness on the social structuring of male 266

dolphins seems plausible; previous studies on male associations and relatedness of 2nd-order alliances reported 267

ambiguous patterns, with only a minority of alliances showing higher relatedness than the population average 268

(55). 269

The high social affinity among male spongers could either indicate social learning of tool use from 270

alliance partners or be explained by homophilous behaviour (i.e., increased associations due to similar 271

behaviour). The established pattern of strict vertical transition of sponging (18,23) and the reported homophily 272

related to sponging in female dolphins of Shark Bay (22), make homophily among male spongers the more 273

parsimonious explanation. Whether the observed homophily among male spongers is driven by the males 274

themselves or emerges as a by-product of the high social affinity of female spongers (i.e., mothers) remains 275

unknown. Research in eastern Shark Bay has shown that juvenile males preferentially stayed in proximity to 276

their natal associates (56), and the number of associates stays constant from infancy through the juvenile 277

period (57). If the natal associates of spongers were also male spongers, this could explain the high social bonds 278

between pairs or trios of sponging males. As sponging females に and hence, mothers of sponging males に are 279

shown to cluster together (22), such a scenario seems plausible. 280

The ultimate benefit of such homophilous behaviour in male spongers could be their ability to 281

maintain the use of such a foraging technique whilst simultaneously remaining in close proximity to males 'of a 282

similar ilk', i.e., with whom they can also engage in alliance behaviours. This argument is further strengthened 283

when considering the composition of 2nd-order alliances. There was only one mixed 2nd-order alliance, while 284

the other eight alliances in our data set consisted of either only male spongers or male non-spongers. The 285

threshold resulting from our PELT analysis to identify 2nd-order alliances was higher than previously 286

documented in Shark Bay (29), resulting in the delineation of a greater number of alliances with some having 287

fewer members than typically reported for 2nd-order alliances (27,29). The higher threshold of 0.27 may have 288

split some 2nd-order alliances that associated at levels of >0.20 but <0.27. Thus, the smaller 2nd-order alliances 289

identified in our study comprising only two to three males are most likely 1st-order allies. Yet, irrespective of 290

the threshold used to define alliances, when considering the hierarchical structure of the social network (i.e., 291

dyadic associations assorted in a dendrogram, Fig. 2), social homophily is apparent. Given the need to 292

synchronise activities when living in groups (i.e., in alliances) (58), males in alliances containing sponging and 293

non-sponging individuals might be at a disadvantage relative to non-mixed alliances. Future research needs to 294

examine whether there are differences in the structure and complexity of 2nd- and 1st-order alliances between 295

male spongers and non-spongers. Here we suggest that the benefits of social homophily may, to a certain 296

extent, mitigate the costs of sponging for male alliance behaviour. 297

Apart from social homophily, behavioural plasticity might manifest itself by allied male spongers 298

reducing the amount of time invested in sponging during the peak mating season, thus further mitigating the 299

costs of being a male sponger to some degree. Nevertheless, the mating season in Shark Bay is only moderately 300

seasonal, with consortships occurring during all months of the year, and a diffuse peak between September 301

and December (59). 302

In summary, we show that while previous assumptions that sponging affects male activity budgets and 303

social pattern hold true, this might not necessarily stand in conflict with male alliance behaviour. The apparent 304

cost mitigating behaviours together with the observed absence of differences in socialising proportions 305

between male spongers and non-spongers weaken the hypothesis that sponging stands in conflict with male 306

alliance behaviour and thereby leading to a female bias in sponging. In fact, preliminary data suggest rates of 307

female monopolisation do not differ between male spongers and male non-spongers (unpublished data). 308

Future research might explore the costs of sponging and how it might be mitigated in more detail, leaving room 309

for other plausible explanations regarding the female bias in social learning of sponging. For instance, time 310

constraints on a male dolphin during its early life may play an important role. Males are weaned earlier than 311

females (60), and therefore have less time to learn sponging from their mothers and, instead, may need to 312

invest time in developing social bonds with other males. Indeed, juvenile male dolphins invest more time in 313

developing social skills than juvenile females, who instead increase their foraging rates (57). In addition, a 314

recent study showed that an extensive training period (decades) is crucial to achieve peak performance in 315

sponging (26). 316

In conclusion, our study explored the impacts of sponging on male dolphin behaviour. We suggest that 317

potential costs associated with sponging for male dolphins might be mitigated by social homophily. Revealing 318

social homophily in bottlenose dolphins is interesting, as in humans, homophilous behaviour is a key factor in 319

the emergence and maintenance of subcultures (61) and the establishment of attachment and close 320

friendships (62). Our study thereby provides another example of convergence in social complexity, innovation 321

and cultural behaviour between cetaceans and great apes (20,22,63,64). 322

323

ACKNOWLEDGEMENTS 324

We thank Shark Bay Resources and the Useless Loop community for their generous, long-term, in-kind and 325

logistical support. We also thank all field assistants for their help during this study. 326

327

DATA ACCESSIBILITY AND DATA CITATION 328

All used datasets are available as electronic supplementary material to this study. 329

330

FUNDING 331

This study was supported by a Swiss National Science Foundation grant (31003A_149956) to M.K. Further 332

financial assistance was provided by grants from the National Geographic Society, W.V. Scott Foundation, 333

SeaWorld Research and Rescue Foundation Inc., A.H. Schultz Stiftung, and the University of Zurich. S.L.K. was 334

supported by The Branco Weiss FellowshipねSociety in Science. W.R.F. was supported by a Graduate 335

Fellowship in Anthropogeny from the University of California, San Diego. 336

337

REFERENCES 338 1. Laland K, Janik V. The animal cultures debate. Trends Ecol Evol [Internet]. 2006 Oct;21(10):542に7. Available from: 339

http://dx.doi.org/10.1016/j.tree.2006.06.005 340 2. Leadbeater E, Chittka L. Social Learning in Insects - From Miniature Brains to Consensus Building [Internet]. Current 341

Biology. 2007. p. R703に13. Available from: https://doi.org/10.1016/j.cub.2007.06.012 342 3. Hoppitt W, Laland KN. Chapter 3 Social Processes Influencing Learning in Animals: A Review of the Evidence 343

[Internet]. Advances in the Study of Behavior. Academic Press; 2008. p. 105に65. Available from: 344 http://dx.doi.org/10.1016/S0065-3454(08)00003-X 345

4. Fogarty L, Laland KN, Morgan TJH, Webster MM, Hoppitt WJE, Rendell L. Cognitive culture: theoretical and 346 empirical insights into social learning strategies. Trends Cogn Sci [Internet]. Elsevier Ltd; 2011;15(2):68に76. 347 Available from: http://dx.doi.org/10.1016/j.tics.2010.12.002 348

5. Giraldeau L, Valone TJ, Templeton JJ. Potential disadvantages of using socially acquired information. Philos Trans R 349 Soc Lond B Biol Sci [Internet]. 2002;357(1427):1559に66. Available from: http://dx.doi.org/10.1098/rstb.2002.1065 350

6. Laland KN. Social learning strategies. Anim Learn Behav [Internet]. 2011;32(1):4に14. Available from: 351 http://dx.doi.org/10.3758/bf03196002 352

7. Pike TW, Laland KN. Conformist learning in nine-ゲヮｷﾐWS ゲデｷIﾆﾉWH;Iﾆゲげ aﾗヴ;ｪｷﾐｪ SWIｷゲｷﾗﾐゲく Bｷﾗﾉ LWデデ ぷIﾐデWヴﾐWデへく 353 2010;6(4):466に8. Available from: http://dx.doi.org/10.1098/rsbl.2009.1014 354

8. Henrich J, Henrich N. The evolution of cultural adaptations: Fijian food taboos protect against dangerous marine 355 toxins. Proc R Soc B Biol Sci [Internet]. The Royal Society; 2010;277(1701):3715に24. Available from: 356 https://doi.org/10.1098/rspb.2010.1191 357

9. Kendal JR, Rendell L, Pike TW, Laland KN. Nine-spined sticklebacks deploy a hill-climbing social learning strategy. 358 Behav Ecol [Internet]. 2009;20(2):238に44. Available from: http://dx.doi.org/10.1093/beheco/arp016 359

10. Hoppitt W, Laland KN. Social learning: an introduction to mechanisms, methods, and models [Internet]. Princeton 360 University Press; 2013. Available from: https://doi.org/10.1016/j.tics.2010.12.002 361

11. Tヴｷ┗Wヴゲ ‘Lく P;ヴWﾐデ;ﾉ ｷﾐ┗WゲデﾏWﾐデ ;ﾐS ゲW┝┌;ﾉ ゲWﾉWIデｷﾗﾐく Iﾐ け“W┝┌;ﾉ “WﾉWIデｷﾗﾐ ;ﾐS デｴW DWゲIWﾐデ ﾗa M;ﾐ ヱΒΑヱにヱΓΑヱげくふESく 362 B. Campbell.) pp. 136に179. Aldine: Chicago, IL; 1972. 363

12. Bateman AJ. Intra-Sexual Selection in Drosophila. Heredity (Edinb). 1984;2:349に68. 364 13. Lonsdorf E V. Sex differences in the development of termite-fishing skills in the wild chimpanzees, Pan troglodytes 365

schweinfurthii, of Gombe National Park, Tanzania. Anim Behav [Internet]. 2005 Sep;70(3):673に83. Available from: 366 http://dx.doi.org/10.1016/j.anbehav.2004.12.014 367

14. Lonsdorf E V, Anderson KE, Stanton MA, Shender M, Heintz MR, Goodall J, et al. Boys will be boys: Sex differences 368 in wild infant chimpanzee social interactions. Anim Behav [Internet]. Elsevier Ltd; 2014 Feb;88:79に83. Available 369 from: http://dx.doi.org/10.1016/j.anbehav.2013.11.015%0A 370

15. Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, Pusey AE. Male dominance rank and 371 reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav [Internet]. 2009 Apr;77(4):873に372 85. Available from: http://dx.doi.org/10.1016/j.anbehav.2008.12.014 373

16. Gilby IC, Brent LJN, Wroblewski EE, Rudicell RS, Hahn BH, Goodall J, et al. Fitness benefits of coalitionary aggression 374 in male chimpanzees. Behav Ecol Sociobiol [Internet]. 2013 Mar 1;67(3):373に81. Available from: 375 http://link.springer.com/10.1007/s00265-012-1457-6 376

17. Smolker R, Richards A, Connor R, Mann J, Berggren P. Sponge Carrying by Dolphins (Delphinidae, Tursiops sp.): A 377 Foraging Specialization Involving Tool Use? Ethology [Internet]. 2010;103(6):454に65. Available from: 378 http://dx.doi.org/10.1111/j.1439-0310.1997.tb00160.x 379

18. Krützen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB. Cultural transmission of tool use in bottlenose 380 dolphins. Proc Natl Acad Sci [Internet]. 2005;102(25):8939に43. Available from: 381 https://doi.org/10.1073/pnas.0500232102 382

19. Patterson EM, Mann J. The ecological conditions that favor tool use and innovation in wild bottlenose dolphins 383 (Tursiops sp.). Brosnan SF, editor. PLoS One [Internet]. 2011 Jul 20;6(7):e22243. Available from: 384 https://dx.plos.org/10.1371/journal.pone.0022243 385

20. Krützen M, Kreicker S, MacLeod CD, Learmonth J, Kopps AM, Walsham P, et al. Cultural transmission of tool use by 386 Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche. Proc R Soc B Biol Sci 387 [Internet]. 2014;281(1784):20140374. Available from: https://doi.org/10.1098/rspb.2014.0374 388

21. Kopps AM, Krützen M, Allen SJ, Bacher K, Sherwin WB. Characterizing the socially transmitted foraging tactic 389 さゲヮﾗﾐｪｷﾐｪざ H┞ HﾗデデﾉWﾐﾗゲW Sﾗﾉヮｴｷﾐゲ ふT┌ヴゲｷﾗヮゲ ゲヮくぶ ｷﾐ デｴW ┘WゲデWヴﾐ ｪ┌ﾉa ﾗa “ｴ;ヴﾆ B;┞が WWゲデWヴﾐ A┌ゲデヴ;ﾉｷ;く Mar Mammal 390 Sci [Internet]. 2014 Jul;30(3):847に63. Available from: http://dx.doi.org/10.1111/mms.12089 391

22. Mann J, Stanton M a, Patterson EM, Bienenstock EJ, Singh LO. Social networks reveal cultural behaviour in tool-392 using using dolphins. Nat Commun [Internet]. Nature Publishing Group; 2012 Jan;3:980. Available from: 393 http://dx.doi.org/10.1038/ncomms1983 394

23. Bacher K, Allen S, Lindholm a K, Bejder L, Krützen M. Genes or Culture: Are mitochondrial genes associated with 395 tool use in bottlenose dolphins (Tursiops sp.)? Behav Genet [Internet]. 2010 Sep;40(5):706に14. Available from: 396 http://dx.doi.org/10.1007/s10519-010-9375-8 397

24. Mann J, Sargeant BL, Watson-Capps JJ, Gibson QA, Heithaus MR, Connor RC, et al. Why do dolphins carry sponges? 398 PLoS One [Internet]. 2008 Jan;3(12):e3868. Available from: http://dx.doi.org/10.1371/journal.pone.0003868 399

25. Mann J, Patterson EM. Tool use by aquatic animals. Phil Trans R Soc B. 2013;368:20120424. 400 26. Patterson EM, Krzyszczyk E, Mann J. Age-specific foraging performance and reproduction in tool-using wild 401

bottlenose dolphins. Behav Ecol [Internet]. 2016;27(2):401に10. Available from: 402

http://dx.doi.org/10.1093/beheco/arv164 403 27. Connor RC, Krützen M. Male dolphin alliances in Shark Bay: Changing perspectives in a 30-year study. Anim Behav 404

[Internet]. 2015;103:223に35. Available from: http://dx.doi.org/10.1016/j.anbehav.2015.02.019 405 28. Connor RC, Wells RJ, Mann J, Read A. Cetacean societies: field studies of dolphins and whales. In: Mann J, Connor 406

R, Tyack P, Whitehead H, editors. University of Chicago Press; 2000. 407 29. Connor RC, Smolker RA, Richards AF. Two levels of alliance formation among male bottlenose dolphins (Tursiops 408

sp.). Proc Natl Acad Sci [Internet]. 1992;89(3):987に90. Available from: http://dx.doi.org/10.1073/pnas.89.3.987 409 30. Gerber L, Connor RC, King SL, Allen SJ, Wittwer S, Bizzozzero MR, et al. Multi-level cooperation in wild male 410

bottlenose dolphins is predicted by long-term friendships. Bevioural Ecol (in Rev). 2019; 411 31. Tyne JA, Loneragan NR, Kopps AM, Allen SJ, Krützen M, Bejder L. Ecological characteristics contribute to sponge 412

distribution and tool use in bottlenose dolphins Tursiops sp. Mar Ecol Prog Ser [Internet]. 2012 Jan;444:143に53. 413 Available from: http://dx.doi.org/10.3354/meps09410 414

32. Würsig B, Würsig M. The Photographic Determination of Group Size, Composition, and Stability of Coastal 415 Porpoises (Tursiops truncatus). Science (80- ) [Internet]. 1977 Nov 18;198(4318):755に6. Available from: 416 http://science.sciencemag.org/content/198/4318/755.abstract 417

33. Smolker RA, Richards AF, Connor RC, Pepper JW. Sex Differences in Patterns of Association among Indian Ocean 418 Bottlenose Dolphins. Behaviour [Internet]. 1992;123(1に2):38に69. Available from: 419 https://doi.org/10.1163/156853992X00101 420

34. Krützen M, Barre L, Möller L, Heithaus M, Simms C, Sherwin W. A biopsy system for small cetaceans: darting 421 success and wound healing in Tursiops spp. Mar Mammal Sci [Internet]. 2002;18(4):863に78. Available from: 422 https://doi.org/10.1111/j.1748-7692.2002.tb01078.x 423

35. Gilson A, Syvanen M, Levine K, Banks J. Deer gender determination by polymerase chain reaction: Validation study 424 and application to tissues, bloodstains, and hair forensic samples from California. Calif Fish Game. 1998;84(4):159に425 69. 426

36. R Core Team. A Language and Environment for Statistical. Computing [Internet]. Vienna; 2013;1:12に21. Available 427 from: http://www.r-project.org 428

37. Mann J, Connor RC, Barré LM, Heithaus MR. Female reproductive success in bottlenose dolphins (Tursiops sp.): life 429 history, habitat, provisioning, and group-size effects. Behav Ecol [Internet]. 2000;11(2):210に9. Available from: 430 http://dx.doi.org/10.1093/beheco/11.2.210 431

38. Connor RC, Smolker R, Bejder L. Synchrony, social behaviour and alliance affiliation in Indian Ocean bottlenose 432 dolphins, Tursiops aduncus. Anim Behav [Internet]. 2006 Dec;72(6):1371に8. Available from: 433 http://dx.doi.org/10.1016/j.anbehav.2006.03.014 434

39. Tabachnick BG, Fidell LS, Ullman JB. Using multivariate statistics. Pearson Boston, MA; 2007. 435 40. Welch WJ. Construction of permutation tests. J Am Stat Assoc [Internet]. 1990;85(411):693に8. Available from: 436

https://doi.org/10.1080/01621459.1990.10474929 437 41. Fay M., Shaw PA. Exact and Asymptotic Weighted Logrank Tests for Interval Censored Data: The interval R Package. 438

J Stat Softw [Internet]. 2010;36(2):1に34. Available from: http://www.jstatsoft.org/v36/i02/ 439 42. Cairns SJ, Schwager SJ. A comparison of association indices. Anim Behav [Internet]. 1987;35(5):1454に69. Available 440

from: https://doi.org/10.1016/S0003-3472(87)80018-0 441 43. Bejder L, Fletcher D, Bräger S. A method for testing association patterns of social animals. Anim Behav [Internet]. 442

1998 Sep;56(3):719に25. Available from: http://dx.doi.org/10.1006/anbe.1998.0802 443 44. Whitehead H, Bejder L, Ottensmeyer CA. Testing association patterns: Issues arising and extensions. Anim Behav 444

[Internet]. Academic Press; 2005;69(5):e1. Available from: http://dx.doi.org/10.1016/j.anbehav.2004.11.004 445 45. Whitehead H. SOCPROG: program for analyzing social structure. Behav Ecol Sociobiol [Internet]. 2009;63(5):765に446

78. Available from: http://dx.doi.org/10.1007/s00265-008-0697-y%0A 447 46. Dekker D, Krackhardt D, Snijders TAB. Sensitivity of MRQAP tests to collinearity and autocorrelation conditions. 448

Psychometrika [Internet]. 2007;72(4):563に81. Available from: https://doi.org/10.1007/s11336-007-9016-1 449 47. Farine DR. Animal social network inference and permutations for ecologists in {R} using asnipe. Methods Ecol Evol 450

[Internet]. 2013;4(12):1187に94. Available from: 451 https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/2041-210X.12121 452

48. Kopps AM, Ackermann CY, Sherwin WB, Allen SJ, Bejder L, Krützen M. Cultural transmission of tool use combined 453 with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins. Proc R Soc B Biol Sci 454 [Internet]. 2014;281(1782):20133245. Available from: https://doi.org/10.1098/rspb.2013.3245 455

49. Whitehead H. Analyzing animal societies: quantitative methods for vertebrate social analysis [Internet]. Chicago: 456 University of Chicago Press; 2008. 161-168 p. Available from: 457 http://public.eblib.com/choice/publicfullrecord.aspx?p=408184. 458

50. KｷﾉﾉｷIﾆ ‘が H;┞ﾐWゲ Kが EIﾆﾉW┞ Iが FW;ヴﾐｴW;S Pが LWW Jく さIｴ;ﾐｪWヮﾗｷﾐデざぎ MWデｴﾗSゲ aﾗヴ Cｴ;ﾐｪWヮﾗｷﾐデ DWデWIデｷﾗﾐ ぷIﾐデWヴﾐWデへく 459 2016. Available from: https://cran.r-project.org/web/packages/changepoint/changepoint.pdf 460

51. King SL, Friedman WR, Allen SJ, Gerber L, Jensen FH, Wittwer S, et al. Bottlenose Dolphins Retain Individual Vocal 461 Labels in Multi-level Alliances. Curr Biol [Internet]. Elsevier; 2018; Available from: 462 https://doi.org/10.1016/j.cub.2018.05.013 463

52. Bridge PD. Classification. In: Fry J, editor. Biological data analysis. Oxford, UK: Oxford University Press; 1993. p. 464 219に42. 465

53. Smith TB, Skúlason S. Evolutionary Significance of Resource Polymorphisms in Fishes , Amphibians , and Birds. Annu 466 Rev Ecol Syst [Internet]. 1996;27(1):111に33. Available from: http://dx.doi.org/10.1146/annurev.ecolsys.27.1.111 467

54. Bolnick DI. Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature [Internet]. 468 2001;410(6827):463に6. Available from: http://dx.doi.org/10.1038/35068555 469

55. Krützen M, Sherwin WB, Connor RC, Barré LM, Van De Casteele T, Mann J, et al. Contrasting relatedness patterns in 470 bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proceedings of the Royal Society B: Biological 471 Sciences [Internet]. 2003. p. 497に502. Available from: http://dx.doi.org/10.1098/rspb.2002.2229 472

56. Tsai YJJ, Mann J. Dispersal, philopatry, and the role of fission-fusion dynamics in bottlenose dolphins. Mar Mammal 473 Sci [Internet]. 2012;29(2):261に79. Available from: http://dx.doi.org/10.1111/j.1748-7692.2011.00559.x 474

57. Krzyszczyk E, Patterson EM, Stanton MA, Mann J. The transition to independence: sex differences in social and 475 behavioural development of wild bottlenose dolphins. Anim Behav [Internet]. Elsevier; 2017;129:43に59. Available 476 from: https://doi.org/10.1016/j.anbehav.2017.04.011 477

58. Tosi CH, Ferreira RG. Differences between solitary and group time budgets in Guiana dolphin (Sotalia guianensis) at 478 northeastern Brazil. Dolphins anatomy, Behav Threat Nov Sci Hauppauge. 2010;197に206. 479

59. “ﾏﾗﾉﾆWヴ ‘Aが Cﾗﾐﾐﾗヴ ‘Cく さPﾗヮざ GﾗWゲ デｴW Dﾗﾉヮｴｷﾐぎ ; VﾗI;ﾉｷ┣;デｷﾗﾐ M;ﾉW BﾗデデﾉWﾐﾗゲW Dﾗﾉヮｴｷﾐゲ PヴﾗS┌IW D┌ヴｷﾐｪ 480 Consortships. Behaviour [Internet]. 1996;133(9に10):643に62. Available from: 481 http://dx.doi.org/10.1163/156853996X00404 482

60. Mann J, Sargeant BL. Like mother like calf: The ontogeny of foraging traditions in wild Indian Ocean bottlenose 483 dolphins (Tursiops sp.). In: Fragaszy DM, Perry S, editors. The Biology of Traditions. Cambridge University Press; 484 2003. p. 236に66. 485

61. McPherson M, Smith-Lovin L, Cook JM. Birds of a Feather: Homophily in Social Networks. Annu Rev Sociol 486 [Internet]. 2001;27(1):415に44. Available from: https://doi.org/10.1146/annurev.soc.27.1.415 487

62. Rivera MT, Soderstrom SB, Uzzi B. Dynamics of Dyads in Social Networks: Assortative, Relational, and Proximity 488 Mechanisms [Internet]. Annual Review of Sociology. 2010. Available from: 489 http://dx.doi.org/10.1146/annurev.soc.34.040507.134743 490

63. Allen SJ, King SL, Krützen M, Brown AM. Multi-modal sexual displays in Australian humpback dolphins. Sci Rep 491 [Internet]. 2017;7(1):1に8. Available from: http://dx.doi.org/10.1038/s41598-017-13898-9 492

64. Lonsdorf E V., Eberly LE, Pusey AE. Sex differences in learning in chimpanzees. Nature [Internet]. 2004 493 Apr;428(6984):715に6. Available from: https://doi.org/10.1038/428715a 494

65. Csárdi G, Nepusz T. The igraph software package for complex network research. J Comput Appl [Internet]. 495 2014;Complex Sy:9. Available from: 496 http://pub.chinasciencejournal.com/JournalofComputerApplications/5970.jhtml 497

498

FIGURE CAPTIONS 499 500 Fig. 1: Social network of the male dolphins in the restricted data set (n = 37). The nodes represent individuals 501 and are shaded according to foraging technique. Edges (lines) below 0.27 HWI are transparent and edge 502 thickness corresponds to edge weight (see Figure S2 for the social network showing all edges). The graph was 503 plotted with the force directed Fruchterman-Reingold algorithm implemented in the けigraphげ package (65). 504 505 506 Fig. 2: Hierarchical cluster diagram based on dyadic HWI measures. A HWI value of 0.27 was used as a cut-off 507 value (grey line) to define communities (i.e., 2nd-order alliances). 508 509 510

TABLES

Tab. 1: Post-hoc, Bonferroni corrected t-tests on activity proportions of male spongers (n = 12) and non-

spongers (n = 20). Significant p- values are indicated in bold print.

proportion spongers non-spongers

t (df)(df) r p Mean SD Mean SD

forage 0.45 0.02 0.20 0.02 -9.42 (26.31) 0.89 < 0.001

rest 0.18 0.01 0.28 0.01 4.83 (27.80) 0.68 < 0.001

travel 0.16 0.02 0.31 0.02 4.83 (27.36) 0.68 < 0.001

socialise 0.16 0.01 0.13 0.01 -1.62 (29.99) 0.28 0.23

Tab. 2: Mean association indices (HWI) by foraging technique of male spongers (n = 13) and non-spongers (n =

24), 666 dyadic relationships.

pair composition mean HWI (SD)

sponger に sponger 0.21 (0.11)

non-sponger に non-sponger 0.10 (0.05)

similar foraging technique 0.14 (0.09)

different foraging technique 0.05 (0.04)

overall 0.09 (0.04)

Tab. 3: MRQAP-DSP model including only genotyped males (n = 25, 300 dyadic relationships). Significant p-

values are indicated in bold print.

variable coefficient p

sponger similarity 0.19 <0.001

non-sponger similarity 0.10 <0.01

relatedness 0.21 0.24

F(3, 297) = 34.5, adjusted R2 = 0.25, p-value < 0.001